Cognitive Impairment in Neurodegenerative Movement Disorders

Abstract

Patients with neurodegenerative movement disorders can develop cognitive impairment during the disease. Cognitive symptoms have been associated with decreased quality of life, higher caregiver burden, and earlier institutionalization, and are therefore critical for physicians to understand and address. The evaluation of cognitive performance of patients with neurodegenerative movement disorders is important for providing adequate diagnosis, management, prognosis, and support patients and their caregivers. In this review, we discuss the features of the cognitive impairment profile of commonly encountered movement disorders: Parkinson's disease, dementia with Lewy bodies, multiple system atrophy, progressive supranuclear palsy, corticobasal syndrome, and Huntington's disease. In addition, we provide neurologists with practical guidance and evaluation tools for the assessment and management of these challenging patients.

Keywords

neurodegenerative movement disorders - cognitive impairment - neuropsychiatric symptoms - dementia

Publication History

Article published online:
20 March 2023

• References

• 1 Roy E. . Cognitive impairment. In: Gellman MD, Turner JR, eds. Encyclopedia of Behavioral Medicine. New York, NY: Springer; 2013:449–451
• 2 McKhann GM, Knopman DS, Chertkow H. et al. The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011; 7 (03) 263-269
• 3 Chaudhuri KR, Healy DG, Schapira AHV. National Institute for Clinical Excellence. Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol 2006; 5 (03) 235-245
• 4 Schapira AHV, Chaudhuri KR, Jenner P. Non-motor features of Parkinson disease. Nat Rev Neurosci 2017; 18 (07) 435-450
• 5 Boström F, Jönsson L, Minthon L, Londos E. Patients with dementia with lewy bodies have more impaired quality of life than patients with Alzheimer disease. Alzheimer Dis Assoc Disord 2007; 21 (02) 150-154
• 6 Rongve A, Vossius C, Nore S, Testad I, Aarsland D. Time until nursing home admission in people with mild dementia: comparison of dementia with Lewy bodies and Alzheimer's dementia. Int J Geriatr Psychiatry 2014; 29 (04) 392-398
• 7 Mueller C, Perera G, Rajkumar AP. et al. Hospitalization in people with dementia with Lewy bodies: frequency, duration, and cost implications. Alzheimers Dement (Amst) 2017; 10: 143-152
• 8 Leiknes I, Tysnes OB, Aarsland D, Larsen JP. Caregiver distress associated with neuropsychiatric problems in patients with early Parkinson's disease: the Norwegian ParkWest study. Acta Neurol Scand 2010; 122 (06) 418-424
• 9 Stubendorff K, Aarsland D, Minthon L, Londos E. The impact of autonomic dysfunction on survival in patients with dementia with Lewy bodies and Parkinson's disease with dementia. PLoS One 2012; 7 (10) e45451
• 10 Postuma RB, Berg D, Stern M. et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 2015; 30 (12) 1591-1601
• 11 Martinez-Martin P. The importance of non-motor disturbances to quality of life in Parkinson's disease. J Neurol Sci 2011; 310 (1–2): 12-16
• 12 Santos-García D, de la Fuente-Fernández R. Impact of non-motor symptoms on health-related and perceived quality of life in Parkinson's disease. J Neurol Sci 2013; 332 (1–2): 136-140
• 13 Schrag A, Hovris A, Morley D, Quinn N, Jahanshahi M. Caregiver-burden in parkinson's disease is closely associated with psychiatric symptoms, falls, and disability. Parkinsonism Relat Disord 2006; 12 (01) 35-41
• 14 Jessen F, Amariglio RE, van Boxtel M. et al; Subjective Cognitive Decline Initiative (SCD-I) Working Group. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer's disease. Alzheimers Dement 2014; 10 (06) 844-852
• 15 Litvan I, Goldman JG, Tröster AI. et al. Diagnostic criteria for mild cognitive impairment in Parkinson's disease: Movement Disorder Society Task Force guidelines. Mov Disord 2012; 27 (03) 349-356
• 16 Emre M, Aarsland D, Brown R. et al. Clinical diagnostic criteria for dementia associated with Parkinson's disease. Mov Disord 2007; 22 (12) 1689-1707 , quiz 1837
• 17 Saredakis D, Collins-Praino LE, Gutteridge DS, Stephan BCM, Keage HAD. Conversion to MCI and dementia in Parkinson's disease: a systematic review and meta-analysis. Parkinsonism Relat Disord 2019; 65: 20-31
• 18 Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG. The Sydney multicenter study of Parkinson's disease: the inevitability of dementia at 20 years. Mov Disord 2008; 23 (06) 837-844
• 19 Cholerton B, Weiner MW, Nosheny RL. et al. Cognitive performance in Parkinson's disease in the Brain Health Registry. J Alzheimers Dis 2019; 68 (03) 1029-1038
• 20 Marinus J, Zhu K, Marras C, Aarsland D, van Hilten JJ. Risk factors for non-motor symptoms in Parkinson's disease. Lancet Neurol 2018; 17 (06) 559-568
• 21 Aarsland D, Creese B, Politis M. et al. Cognitive decline in Parkinson disease. Nat Rev Neurol 2017; 13 (04) 217-231
• 22 Purri R, Brennan L, Rick J. et al. Subjective cognitive complaint in Parkinson's disease patients with normal cognition: canary in the coal mine?. Mov Disord 2020; 35 (09) 1618-1625
• 23 Galtier I, Nieto A, Lorenzo JN, Barroso J. Subjective cognitive decline and progression to dementia in Parkinson's disease: a long-term follow-up study. J Neurol 2019; 266 (03) 745-754
• 24 Cholerton BA, Poston KL, Yang L. et al. Semantic fluency and processing speed are reduced in non-cognitively impaired participants with Parkinson's disease. J Clin Exp Neuropsychol 2021; 43 (05) 469-480
• 25 Erro R, Santangelo G, Barone P. et al. Do subjective memory complaints herald the onset of mild cognitive impairment in Parkinson disease?. J Geriatr Psychiatry Neurol 2014; 27 (04) 276-281
• 26 Hong JY, Sunwoo MK, Chung SJ. et al. Subjective cognitive decline predicts future deterioration in cognitively normal patients with Parkinson's disease. Neurobiol Aging 2014; 35 (07) 1739-1743
• 27 Weintraub D, Simuni T, Caspell-Garcia C. et al; Parkinson's Progression Markers Initiative. Cognitive performance and neuropsychiatric symptoms in early, untreated Parkinson's disease. Mov Disord 2015; 30 (07) 919-927
• 28 Pedersen KFLJ, Larsen JP, Tysnes OB, Alves G. Natural course of mild cognitive impairment in Parkinson disease: a 5-year population-based study. Neurology 2017; 88 (08) 767-774
• 29 Domellöf ME, Ekman U, Forsgren L, Elgh E. Cognitive function in the early phase of Parkinson's disease, a five-year follow-up. Acta Neurol Scand 2015; 132 (02) 79-88
• 30 Buter TC, van den Hout A, Matthews FE, Larsen JP, Brayne C, Aarsland D. Dementia and survival in Parkinson disease: a 12-year population study. Neurology 2008; 70 (13) 1017-1022
• 31 Aarsland D, Andersen K, Larsen JP, Lolk A, Nielsen H, Kragh-Sørensen P. Risk of dementia in Parkinson's disease: a community-based, prospective study. Neurology 2001; 56 (06) 730-736
• 32 Phongpreecha T, Cholerton B, Mata IF. et al. Multivariate prediction of dementia in Parkinson's disease. NPJ Parkinsons Dis 2020; 6: 20
• 33 Fengler S, Liepelt-Scarfone I, Brockmann K, Schäffer E, Berg D, Kalbe E. Cognitive changes in prodromal Parkinson's disease: a review. Mov Disord 2017; 32 (12) 1655-1666
• 34 Watson GS, Leverenz JB. Profile of cognitive impairment in Parkinson's disease. Brain Pathol 2010; 20 (03) 640-645
• 35 Rodríguez-Constenla I, Cabo-López I, Bellas-Lamas P, Cebrián E. Cognitive and neuropsychiatric disorders in Parkinson's disease [in Spanish]. Rev Neurol 2010; 50 (2, Suppl 2): S33-S39
• 36 Ballard CG, Aarsland D, McKeith I. et al. Fluctuations in attention: PD dementia vs DLB with parkinsonism. Neurology 2002; 59 (11) 1714-1720
• 37 Goetz CG, Emre M, Dubois B. Parkinson's disease dementia: definitions, guidelines, and research perspectives in diagnosis. Ann Neurol 2008; 64 (Suppl (Suppl. 02) S81-S92
• 38 Revonsuo A, Portin R, Koivikko L, Rinne JO, Rinne UK. Slowing of information processing in Parkinson's disease. Brain Cogn 1993; 21 (01) 87-110
• 39 Szatmari S, Illigens BM, Siepmann T, Pinter A, Takats A, Bereczki D. Neuropsychiatric symptoms in untreated Parkinson's disease. Neuropsychiatr Dis Treat 2017; 13: 815-826
• 40 Compta Y, Martí MJ, Ibarretxe-Bilbao N. et al. Cerebrospinal tau, phospho-tau, and beta-amyloid and neuropsychological functions in Parkinson's disease. Mov Disord 2009; 24 (15) 2203-2210
• 41 Compta Y, Parkkinen L, Kempster P. et al. The significance of α-synuclein, amyloid-β and tau pathologies in Parkinson's disease progression and related dementia. Neurodegener Dis 2014; 13 (2–3): 154-156
• 42 Ryman SG, Yutsis M, Tian L. et al. Cognition at each stage of Lewy body disease with co-occurring Alzheimer's disease pathology. J Alzheimers Dis 2021; 80 (03) 1243-1256
• 43 Linortner P, McDaniel C, Shahid M. et al. White matter hyperintensities related to Parkinson's disease executive function. Mov Disord Clin Pract (Hoboken) 2020; 7 (06) 629-638
• 44 McKeith IG, Boeve BF, Dickson DW. et al. Diagnosis and managament of dementia with Lewy bodies. Neurology 2017; 89 (01) 88-100
• 45 Ferman TJ, Smith GE, Boeve BF. et al. Neuropsychological differentiation of dementia with Lewy bodies from normal aging and Alzheimer's disease. Clin Neuropsychol 2006; 20 (04) 623-636
• 46 Brønnick K, Breitve MH, Rongve A, Aarsland D. Neurocognitive deficits distinguishing mild dementia with Lewy bodies from mild Alzheimer's disease are associated with parkinsonism. J Alzheimers Dis 2016; 53 (04) 1277-1285
• 47 Oda H, Yamamoto Y, Maeda K. The neuropsychological profile in dementia with Lewy bodies and Alzheimer's disease. Int J Geriatr Psychiatry 2009; 24 (02) 125-131
• 48 Walker Z, Allen RL, Shergill S, Katona CL. Neuropsychological performance in Lewy body dementia and Alzheimer's disease. Br J Psychiatry 1997; 170: 156-158
• 49 Hamilton JM, Salmon DP, Galasko D. et al. A comparison of episodic memory deficits in neuropathologically-confirmed Dementia with Lewy bodies and Alzheimer's disease. J Int Neuropsychol Soc 2004; 10 (05) 689-697
• 50 Jellinger KA. Heterogeneity of multiple system atrophy: an update. Biomedicines 2022; 10 (03) 599
• 51 McKeith IG, Galasko D, Kosaka K. et al. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology 1996; 47 (05) 1113-1124
• 52 Donaghy PC, McKeith IG. The clinical characteristics of dementia with Lewy bodies and a consideration of prodromal diagnosis. Alzheimers Res Ther 2014; 6 (04) 46
• 53 Abbate C, Trimarchi PD, Inglese S. et al. Preclinical polymodal hallucinations for 13 years before dementia with Lewy bodies. Behav Neurol 2014; 2014: 694296
• 54 Tiraboschi P, Salmon DP, Hansen LA, Hofstetter RC, Thal LJ, Corey-Bloom J. What best differentiates Lewy body from Alzheimer's disease in early-stage dementia?. Brain 2006; 129 (Pt 3): 729-735
• 55 McKeith IG, Dickson DW, Lowe J. et al; Consortium on DLB. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 2005; 65 (12) 1863-1872
• 56 McKeith IG, Ferman TJ, Thomas AJ. et al; prodromal DLB Diagnostic Study Group. Research criteria for the diagnosis of prodromal dementia with Lewy bodies. Neurology 2020; 94 (17) 743-755
• 57 Gilman S, Wenning GK, Low PA. et al. Second consensus statement on the diagnosis of multiple system atrophy. Neurology 2008; 71 (09) 670-676
• 58 Gilman S, May SJ, Shults CW. et al; North American Multiple System Atrophy Study Group. The North American Multiple System Atrophy Study Group. J Neural Transm (Vienna) 2005; 112 (12) 1687-1694
• 59 Kim HJ, Jeon BS, Kim YE. et al. Clinical and imaging characteristics of dementia in multiple system atrophy. Parkinsonism Relat Disord 2013; 19 (06) 617-621
• 60 Brown RG, Lacomblez L, Landwehrmeyer BG. et al; NNIPPS Study Group. Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain 2010; 133 (Pt 8): 2382-2393
• 61 Siri C, Duerr S, Canesi M. et al. A cross-sectional multicenter study of cognitive and behavioural features in multiple system atrophy patients of the parkinsonian and cerebellar type. J Neural Transm (Vienna) 2013; 120 (04) 613-618
• 62 Sambati L, Calandra-Buonaura G, Giannini G. et al. Cognitive profile and its evolution in a cohort of multiple system atrophy patients. Front Neurol 2020; 11: 537360
• 63 Stankovic I, Krismer F, Jesic A. et al; Movement Disorders Society MSA (MODIMSA) Study Group. Cognitive impairment in multiple system atrophy: a position statement by the Neuropsychology Task Force of the MDS Multiple System Atrophy (MODIMSA) study group. Mov Disord 2014; 29 (07) 857-867
• 64 Barcelos LB, Saad F, Giacominelli C. et al. Neuropsychological and clinical heterogeneity of cognitive impairment in patients with multiple system atrophy. Clin Neurol Neurosurg 2018; 164: 121-126
• 65 Bak TH, Caine D, Hearn VC, Hodges JR. Visuospatial functions in atypical parkinsonian syndromes. J Neurol Neurosurg Psychiatry 2006; 77 (04) 454-456
• 66 Wenning GK, Stankovic I, Vignatelli L. et al. The Movement Disorder Society Criteria for the diagnosis of multiple system atrophy. Mov Disord 2022; 37 (06) 1131-1148
• 67 Koga S, Aoki N, Uitti RJ. et al. When DLB, PD, and PSP masquerade as MSA: an autopsy study of 134 patients. Neurology 2015; 85 (05) 404-412
• 68 Burrell JR, Hodges JR, Rowe JB. Cognition in corticobasal syndrome and progressive supranuclear palsy: a review. Mov Disord 2014; 29 (05) 684-693
• 69 Gerstenecker A, Mast B, Duff K, Ferman TJ, Litvan I. ENGENE-PSP Study Group. Executive dysfunction is the primary cognitive impairment in progressive supranuclear palsy. Arch Clin Neuropsychol 2013; 28 (02) 104-113
• 70 Rittman T, Coyle-Gilchrist IT, Rowe JB. Managing cognition in progressive supranuclear palsy. Neurodegener Dis Manag 2016; 6 (06) 499-508
• 71 Zarei M, Pouretemad HR, Bak T, Hodges JR. Autobiographical memory in progressive supranuclear palsy. Eur J Neurol 2010; 17 (02) 238-241
• 72 Höglinger GU, Respondek G, Stamelou M. et al; Movement Disorder Society-endorsed PSP Study Group. Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 2017; 32 (06) 853-864
• 73 Ghosh BC, Carpenter RH, Rowe JB. A longitudinal study of motor, oculomotor and cognitive function in progressive supranuclear palsy. PLoS One 2013; 8 (09) e74486
• 74 Duff K, McDermott D, Luong D, Randolph C, Boxer AL. Cognitive deficits in progressive supranuclear palsy on the Repeatable Battery for the Assessment of Neuropsychological Status. J Clin Exp Neuropsychol 2019; 41 (05) 469-475
• 75 Armstrong MJ, Litvan I, Lang AE. et al. Criteria for the diagnosis of corticobasal degeneration. Neurology 2013; 80 (05) 490-503
• 76 Mathew R, Bak TH, Hodges JR. Diagnostic criteria for corticobasal syndrome: a comparative study. J Neurol Neurosurg Psychiatry 2012; 83 (04) 405-410
• 77 Pillon B, Blin J, Vidailhet M. et al. The neuropsychological pattern of corticobasal degeneration: comparison with progressive supranuclear palsy and Alzheimer's disease. Neurology 1995; 45 (08) 1477-1483
• 78 Burrell JR, Hornberger M, Villemagne VL, Rowe CC, Hodges JR. Clinical profile of PiB-positive corticobasal syndrome. PLoS One 2013; 8 (04) e61025
• 79 Grimes DA, Lang AE, Bergeron CB. Dementia as the most common presentation of cortical-basal ganglionic degeneration. Neurology 1999; 53 (09) 1969-1974
• 80 Murray R, Neumann M, Forman MS. et al. Cognitive and motor assessment in autopsy-proven corticobasal degeneration. Neurology 2007; 68 (16) 1274-1283
• 81 Belvisi D, Berardelli I, Suppa A. et al. Neuropsychiatric disturbances in atypical parkinsonian disorders. Neuropsychiatr Dis Treat 2018; 14: 2643-2656
• 82 Walker FO. Huntington's disease. Lancet 2007; 369 9557 218-228
• 83 Peavy GM, Jacobson MW, Goldstein JL. et al. Cognitive and functional decline in Huntington's disease: dementia criteria revisited. Mov Disord 2010; 25 (09) 1163-1169
• 84 Keum JW, Shin A, Gillis T. et al. The HTT CAG-expansion mutation determines age at death but not disease duration in Huntington disease. Am J Hum Genet 2016; 98 (02) 287-298
• 85 Andrew SE, Goldberg YP, Kremer B. et al. The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat Genet 1993; 4 (04) 398-403
• 86 Shannon KM. Huntington's disease – clinical signs, symptoms, presymptomatic diagnosis, and diagnosis. Handb Clin Neurol 2011; 100: 3-13
• 87 Anderson KE. Huntington's disease. Handb Clin Neurol 2011; 100: 15-24
• 88 Craufurd D, Thompson JC, Snowden JS. Behavioral changes in Huntington disease. Neuropsychiatry Neuropsychol Behav Neurol 2001; 14 (04) 219-226
• 89 Martinez-Horta S, Perez-Perez J, van Duijn E. et al; Spanish REGISTRY investigators of the European Huntington's Disease Network. Neuropsychiatric symptoms are very common in premanifest and early stage Huntington's disease. Parkinsonism Relat Disord 2016; 25: 58-64
• 90 van Duijn E, Craufurd D, Hubers AA. et al; European Huntington's Disease Network Behavioural Phenotype Working Group. Neuropsychiatric symptoms in a European Huntington's disease cohort (REGISTRY). J Neurol Neurosurg Psychiatry 2014; 85 (12) 1411-1418
• 91 Thompson JC, Harris J, Sollom AC. et al. Longitudinal evaluation of neuropsychiatric symptoms in Huntington's disease. J Neuropsychiatry Clin Neurosci 2012; 24 (01) 53-60
• 92 Hubers AA, Reedeker N, Giltay EJ, Roos RA, van Duijn E, van der Mast RC. Suicidality in Huntington's disease. J Affect Disord 2012; 136 (03) 550-557
• 93 Kachian ZR, Cohen-Zimerman S, Bega D, Gordon B, Grafman J. Suicidal ideation and behavior in Huntington's disease: systematic review and recommendations. J Affect Disord 2019; 250: 319-329
• 94 van Duijn E, Kingma EM, van der Mast RC. Psychopathology in verified Huntington's disease gene carriers. J Neuropsychiatry Clin Neurosci 2007; 19 (04) 441-448
• 95 Nasreddine ZS, Phillips NA, Bédirian V. et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005; 53 (04) 695-699
• 96 Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12 (03) 189-198
• 97 Mattis S. . Dementia Rating Scale: Professional Manual. Florida: Odessa; 1988
• 98 Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a frontal assessment battery at bedside. Neurology 2000; 55 (11) 1621-1626
• 99 Pagonabarraga J, Kulisevsky J, Llebaria G, García-Sánchez C, Pascual-Sedano B, Gironell A. Parkinson's disease-cognitive rating scale: a new cognitive scale specific for Parkinson's disease. Mov Disord 2008; 23 (07) 998-1005
• 100 Wittich W, Phillips N, Nasreddine Z, Chertkow H. Sensitivity and specificity of the Montreal Cognitive Assessment modified for individuals who are visually impaired. J Vis Impair Blind 2010; 104 (06) 360-368
• 101 Berg JL, Durant J, Léger GC, Cummings JL, Nasreddine Z, Miller JB. Comparing the electronic and standard versions of the montreal cognitive assessment in an outpatient memory disorders clinic: a validation study. J Alzheimers Dis 2018; 62 (01) 93-97
• 102 Marras C, Armstrong MJ, Meaney CA. et al. Measuring mild cognitive impairment in patients with Parkinson's disease. Mov Disord 2013; 28 (05) 626-633
• 103 Hendershott TR, Zhu D, Llanes S, Poston KL. Domain-specific accuracy of the Montreal Cognitive Assessment subsections in Parkinson's disease. Parkinsonism Relat Disord 2017; 38: 31-34
• 104 Hoops S, Nazem S, Siderowf AD. et al. Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease. Neurology 2009; 73 (21) 1738-1745
• 105 Kulisevsky J, Pagonabarraga J. Cognitive impairment in Parkinson's disease: tools for diagnosis and assessment. Mov Disord 2009; 24 (08) 1103-1110
• 106 Alegret M, Espinosa A, Vinyes-Junqué G. et al. Normative data of a brief neuropsychological battery for Spanish individuals older than 49. J Clin Exp Neuropsychol 2012; 34 (02) 209-219
• 107 Cholerton B, Poston KL, Tian L. et al. Participant and study partner reported impact of cognition on functional activities in Parkinson's disease. Mov Disord Clin Pract (Hoboken) 2019; 7 (01) 61-69
• 108 Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J. The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology 1994; 44 (12) 2308-2314
• 109 Yesavage JA, Brink TL, Rose TL. et al. Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 1983; 17 (01) 37-49
• 110 Sheikh JI, Yesavage JA. Geriatric Depression Scale (GDS). Recent evidence and development of a shorter version. Clin Gerontol 1986; 5 1–2 165-173
• 111 Spielberger CD, Gorsuch R. , Lushene RE., Vagg PR, Jacobs GA. Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press; 1983
• 112 Wedderburn C, Wear H, Brown J. et al. The utility of the Cambridge Behavioural Inventory in neurodegenerative disease. J Neurol Neurosurg Psychiatry 2008; 79 (05) 500-503
• 113 Goetz CG, Tilley BC, Shaftman SR. et al; Movement Disorder Society UPDRS Revision Task Force. Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 2008; 23 (15) 2129-2170
• 114 Suwijn SR, van Boheemen CJ, de Haan RJ, Tissingh G, Booij J, de Bie RM. The diagnostic accuracy of dopamine transporter SPECT imaging to detect nigrostriatal cell loss in patients with Parkinson's disease or clinically uncertain parkinsonism: a systematic review. EJNMMI Res 2015; 5: 12
• 115 Robinson JL, Lee EB, Xie SX. et al. Neurodegenerative disease concomitant proteinopathies are prevalent, age-related and APOE4-associated. Brain 2018; 141 (07) 2181-2193
• 116 van Steenoven I, Aarsland D, Weintraub D. et al; European DLB consortium. Cerebrospinal fluid Alzheimer's disease biomarkers across the spectrum of Lewy body diseases: results from a large multicenter cohort. J Alzheimers Dis 2016; 54 (01) 287-295
• 117 Abdelnour C, van Steenoven I, Londos E. et al; European DLB Consortium. Alzheimer's disease cerebrospinal fluid biomarkers predict cognitive decline in lewy body dementia. Mov Disord 2016; 31 (08) 1203-1208
• 118 Bellomo G, De Luca CMG, Paoletti FP, Gaetani L, Moda F, Parnetti L. α-Synuclein seed amplification assays for diagnosing synucleinopathies: the way forward. Neurology 2022; 99 (05) 195-205
• 119 Aarsland D, Batzu L, Halliday GM. et al. Parkinson disease-associated cognitive impairment. Nat Rev Dis Primers 2021; 7 (01) 47
• 120 Seppi K, Ray Chaudhuri K, Coelho M. et al; the collaborators of the Parkinson's Disease Update on Non-Motor Symptoms Study Group on behalf of the Movement Disorders Society Evidence-Based Medicine Committee. Update on treatments for nonmotor symptoms of Parkinson's disease-an evidence-based medicine review. Mov Disord 2019; 34 (02) 180-198
• 121 Delis DC, Kramer JH, Kaplan E, Ober BA. . The California Verbal Learning Test: Research edition, adult version. New York, NY: The Psychological Corporation; 1987
• 122 Brandt J. The hopkins verbal learning test: development of a new memory test with six equivalent forms. Clin Neuropsychol 1991; 5 (02) 125-142
• 123 Grober E, Buschke H. Genuine memory deficits in dementia. Dev Neuropsychol 1987; 3 (01) 13-36
• 124 Wechsler D. . Wechsler Memory Scale IV (WMS-IV). New York, NY: Psychological Corporation; 2009
• 125 Smith A. . Symbol Digits Modalities Test. Victoria: Western Psychological Services; 1982
• 126 Freedman M, Leach L, Kaplan E, Winocur G, Shulman KJ, Delis DC. Clock Drawing. Oxford:: Oxford University Press; 1994
• 127 Morris JC, Heyman A, Mohs RC. et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 1989; 39 (09) 1159-1165
• 128 Goodglass H, Kaplan E. . The Assessment of Aphasia and Related Disorders. Philadelphia, PA: Lea and Febiger; 1983
• 129 Spreen O, Benton AL. . Neurosensory Centre Comprehensive Examination for Aphasia: Manual of Directions. Victoria: University of Victoria, Neuropsychology Laboratory; 1969
• 130 Heaton RK, Chelune GJ, Talley JL, Kay GG, Curtis G. . Wisconsin Card Sorting Test Manual: Revised and Expanded. Lutz, FL: Psychological Assessment Resources; 1993.
• 131 Wechsler D. . Wechsler Adult Intelligence Scale—Fourth Edition Administration and Scoring Manual. London: Pearson; 2008
• 132 Overall JE, Schaltenbrand R. The SKT neuropsychological test battery. J Geriatr Psychiatry Neurol 1992; 5 (04) 220-227
• 133 Lehfeld H, Erzigkeit H. The SKT--a short cognitive performance test for assessing deficits of memory and attention. Int Psychogeriatr 1997; 9 (Suppl (Suppl. 01) 115-121
• 134 Battery AIT. Manual of Directions and Scoring. Washington, DC: War Department, Adjutant General's Office; 1944
• 135 Reitan R. . Neuropsychological Test Battery. Tucson, AZ: Reitan Neuropsychology Laboratory; 1955
• 136 Golden C. . The Stroop Color and Word Test: A Manual for Clinical and Experimental Uses. Wood Dale, IL: Stoelting Co; 2002
• 137 Benton AL, Sivan AB, Hamsher K. deS., Varney NR, Spreen O. Contributions to Neuropsychological Assessment: A Clinical Manual. Oxford: Oxford University Press; 1983
• 138 Hooper HE. . Hooper Visual Organization Test (VOT). Victoria: Western Psychological Services; 1983.
• 139 Della Sala S, Laiacona M, Spinnler H, Trivelli C. Poppelreuter-Ghent's Overlapping Figures Test: its sensitivity to age, and its clinical use. Arch Clin Neuropsychol 1995; 10 (06) 511-534
• 140 Colarusso RP, Hammill D. . D. Motor-Free Visual Perception Test-Fourth Edition (MVPT-4). Novato, CA: Academic Therapy Publications, Inc.; 2015
• 141 Kaplan E, Goodglass H, Weintraub S. . Boston Naming Test Scoring Booklet, Experimental Edition. Washington, DC: Veterans Administration Hospital; 1976
• 142 Ivanova I, Salmon DP, Gollan TH. The multilingual naming test in Alzheimer's disease: clues to the origin of naming impairments. J Int Neuropsychol Soc 2013; 19 (03) 272-283
• 143 Howard D. . The Pyramids and Palm Trees Test: A Test of Semantic Access From Words and Pictures. Bury St. Edmunds, Suffolk: Thames Valley Test Company; 1992
• 144 Buschke H. Cued recall in amnesia. J Clin Neuropsychol 1984; 6 (04) 433-440